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Stimulation of Molting and Ovarian Maturation by Methyl Farnesoate in the Pacific White Shrimp Litopenaeus vannamei(Boone, 1931)
Stimulation of Molting and Ovarian Maturation by Methyl Farnesoate in the Pacific White Shrimp Litopenaeus vannamei(Boone, 1931)
Fisheries and aquatic sciences. 2014. Mar, 17(1): 115-121
Copyright © 2014, The Korean Society of Fisheries and Aquatic Science
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial Licens (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : July 07, 2013
  • Accepted : September 09, 2013
  • Published : March 31, 2014
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About the Authors
Tariq Alnawafleh
Bo-Kwang Kim
Hye-Eun Kang
Tae-Ho Yoon
Hyun-Woo Kim
kimhw@pknu.ac.kr
Abstract
Eyestalk ablation (ESA) is commonly used in aquaculture to stimulate ovarian maturation in crustaceans, and methyl farnesoate (MF) affects crustacean molting and reproduction. To investigate the physiological effects of ESA and MF treatments on the shrimp Litopenaeus vannamei , we compared the effects of single eyestalk removal and MF injections. The ESA group had the lowest survival rate (50%), and individuals in the 0.1 μg and 1.0 μg MF-treated groups had survival rates of 80 and 73.3%, respectively. Conversely, molting numbers were highest in the ESA group, and similar to those of the 1.0-μg MF group. To investigate shrimp growth, we measured body weight during the experimental period and found that individuals in the ESA and 1.0 μg MF groups showed significant increases in body weight. Furthermore, to investigate the effects of ESA and MF treatments on gonadal maturation, the gonad somatic index (GSI) was calculated after the experiment. All treated groups (ESA and MF) had higher GSI values than the control group, but the ESA and 1.0 μg MF groups were not significantly different. Using histological ovary analysis, we determined that all treated groups showed indications of the previtellogenic stage, unlike the control group (immature stage). These results suggest that the high-MF-concentration treatment produced effects similar to those of ESA with respect to molting number, growth, and ovarian maturation.
Keywords
Introduction
Manipulating reproduction is a major challenge in crustacean aquaculture. Single-eyestalk ablation (ESA) is currently the only strategy used to induce gonad development and spawning in crustacean aquaculture farms ( Choy, 1987 ; Emmerson, 1980 ), and is based on the hormonal physiology of decapod crustaceans. Molting and reproduction are regulated mainly by ecdysteroids, especially 20-hydroxyecdysone (20E), which is produced by the Y-organ ( Nakatsuji et al., 2009 ). The eyestalk ganglia contain the X-organ/sinus gland (XO-SG) complex, which produces a molt-inhibiting hormone (MIH). As a member of the crustacean hyperglycemic hormone (CHH) subfamily II, the MIH peptide hormone acts on the Y-organ, suppressing 20E synthesis ( Covi et al., 2009 ; Nakatsuji et al., 2009 ; Mykles, 2011 ; Nagaraju, 2011 ). As the result of ESA, inhibitory factors, including MIH, are removed, increasing 20E production and up-regulating its physiological response. Although ESA is an effective strategy for inducing maturation, the high death rates following surgical procedures, and lower healthy seed ratios, remain major problems ( Emmerson, 1980 ; Choy, 1987 ); thus, a better strategy must be developed.
Methyl farnesoate (MF) is a sesquiterpenoid compound found in decapod crustaceans, and is structurally similar to the juvenile hormone (JH) of insects. However, MF differs from juvenile hormone (JH III) in containing an epoxide moiety at the terminal end ( Fig. 1 ). Crustaceans appear to lack epoxidase and S-adenosyl-methionine-dependent methyltransferase, which convert farnesoic acid (FA) to JH III ( Hui et al., 2010 ). Therefore, crustaceans lack JH III, and MF is the end product of sesquiterpenoid biosynthesis. In insects, JH III is the major hormone related to metamorphosis, gonad maturation, and molting ( Belles et al., 2005 ; Tsubota et al., 2010 ). Since its discovery in the mandibular organ (MO) in crustaceans ~25 years ago, research has accumulated and authors have proposed that MF acts as a crustacean hormone ( Borst et al., 1987 ; Laufer et al., 1987 ; Nagaraju, 2007 ). The major production site for MF is MO, and its biosynthesis is negatively controlled by the mandibular organ-inhibiting hormone (MOIH), secreted from the XO-SG complex at the terminal end of the eyestalk ( Borst et al., 2001 ; Nagaraju et al., 2003 , 2005 ). The MOIH peptide hormone suppresses the production of MF.
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Chemical structures of methyl farnesoate (MF) and juvenile hormone III (JH III).
Previous studies have suggested that MF treatment results in a physiological response similar to that to 20E in decapod crustaceans. Several studies showed that MF stimulates gonadal development in crustaceans ( Wainwright et al., 1996 ; Homola and Chang, 1997 ; Borst et al., 2002 ; Nagaraju, 2007 ). In addition, MF treatment causes molt acceleration in several crustacean species, such as the crayfish Procambarus clarkii ( Laufer et al., 2005 ) and the freshwater crab Oziotelphusa senex senex ( Reddy et al., 2004 ). However, the effects varied among species, and no consensus has yet been reached.
The main goal of this study was to compare the chronic effects of MF treatment and ESA on the growth and ovarian maturation of the shrimp Litopenaeus vannamei . We evaluated molt frequency, growth rate, and gonadosomatic index (GSI) index after injection of 0.1- and 1.0-μg MF and unilateral ESA for 1 month. Histological analysis was also performed to compare the reproductive stages in the experimental groups.
Materials and Methods
- Animals
Live Litopenaeus vannamei individuals were purchased from a local market in Busan, South Korea. Before the experiment, shrimp were acclimatized for 1 week in plastic tanks (700 L/m 3 ) of seawater, with circulating aeration. Temperature (28 ± 0.5℃) was maintained with a thermostat (Ami Co., Korea), and salt concentration (34 ± 1 psu) was adjusted using distilled water or filtered seawater daily, without exchanging water. To remove nitrogenous compounds, SRO-500EXT skimmer (REEF OCTOPUS, Shanghai ,China) was used for water circulation. The laboratory photoperiod was kept at 10-h light:14-h dark. Animals were fed a frozen diet composed of 50% polychaete worms and 50% squid once daily, which accounted for a total of 5% of the animals’ wet weight biomass, adjusted daily. Feces and unconsumed feed were removed from the tanks daily.
- MF treatment and biological measurement
We produced a stock solution of MF (Echelon Biosciences, Salt Lake City, UT, USA), following Nagaraju and Borst(2008) . The solution was aliquoted and stored at –20℃ before use. Sixty immature adult shrimp (body weight [BW] 21.22 ± 1.48 g, mean ± SD) were divided randomly into four groups (15 individuals per group): control, ESA, 0.1-μg MF, and 1.0-μg MF. Eyestalks were removed and wounds were cauterized to minimize hemolymph loss, as described by Salma et al. (2012) . The MF solutions were injected into shrimp on days 1, 8, 15, 22, and 29. To calculate survival rate, we removed dead individuals from each experimental group, and to calculate molt frequency, we removed molted shells from tanks, on a daily basis.
After 31 days of culture, individuals in each group were dissected immediately following BW measurement. Survival rate was calculated as the final number of live shrimp × 100/the initial number of shrimp. The BW gain was calculated by comparing the final and initial BWs of individuals. To investigate maturation, we calculated the GSI, as follows. The reproductive organs (ovaries) in the cephalothorax were dissected, following Bell and Lightner (1988) , and wet weights were recorded. The GSI was calculated using the standard formula:
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- Histological analysis
To understand maturation stages, three gonads from each group were subjected to histological analysis. The dissected gonads were fixed in Bouin’s fixative for 1 day and washed in running tap water. After washing, the samples were dehydrated in a gradient alcohol series, and embedded in paraffin. The paraffin blocks were trimmed and then sectioned (5 μm) with a microtome. Sections were stained with Harris’ hematoxylin and eosin, and mounted on a slide using marynol (Muto Pure Chemicals Co., Tokyo, Japan). The developmental stage was divided into the following four categories, following Tinikul et al. (2011) : 1) early previtellogenic oocytes, 2) late previtellogenic oocytes, 3) early vitellogenic oocytes, and 4) mature oocytes.
- Statistical analysis
For statistical analysis, we used Student’s t -test (α = 0.05), in SigmaPlot, version 10.1.
Results and Discussion
- Effects of treatments on survival rate, molting and growth
To investigate the effects of ESA and MF treatments, survival rate and molt frequency were calculated after 31 days of culture ( Table 1 ). Survival rate was highest in the control group (90%), followed by MF-treated groups (73.3% for 1.0 μg and 80% for 0.1 μg). The highest mortality occurred in the ESA group (50%), in which six individuals died within 24 h, supporting the notion that physical amputation is a direct cause of death. Although ESA is commonly used for ovarian maturation ( Browdy, 1992 ), it has negative effects on survival. Unilateral ESA is an accepted alternative method of improving survival rates ( Ponnuchamy et al., 1981 ), but rates vary among species; e.g., Panulirus ornatus ( Juinio-Meñez and Ruinata, 1996 ), Penaeus monodon ( Santiago, 1977 ), and Penaeus japonicas ( Yano, 1984 ). This variation may have arisen from species-specific characteristics or the skill levels of experimenters in performing ESA. In this study, injections of MF resulted in higher survival rates than ESA, suggesting that MF injection is relatively safer.
Effects of MF and unilateral ESA on survival and molting ofLitopenaeus vannamei
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MF, methyl farnesoate; ESA, eyestalk ablation.
Individuals in the ESA group showed the highest rate of molting, almost double that of the control group ( Table 1 ). Groups treated with MF had a higher frequency of molting than did the control group, and shrimp treated with 1.0 μg of MF showed a frequency of molting similar to that of the ESA group, indicating that MF injection facilitates molting, similar to the effects of ESA. Several previous studies have proposed that MF is associated with crustacean molting. For example, in Procambarus clarkia , the MF concentration increased during the pre-molt stage and decreased during the post-molt stage, similar to the ecdysteroid concentration pattern ( Laufer et al., 2005 ). Additionally, MF injection accelerated molting in both female and male crabs, Oziotelphusa senex senex ( Reddy et al., 2004 ). Finally, Abdu et al. (2001) found that feeding Cherax quadricarinatus females MF also increased molting frequency ( Abdu et al., 2001 ). Although the precise mechanism is unknown, these findings support the association of MF with crustacean molting.
Finally, we evaluated BW gain during the experimental period ( Fig. 2 ). Final BWs in the 1.0-μg MF and ESA groups were significantly different from the initial values ( P < 0.01). There was no significant difference in BW between the 0.1-μg MF and control groups. The increased growth in the 1.0-μg MF and ESA groups may have resulted from the higher frequency of molting. As in other arthropods, growth in decapods is discontinuous and the greatest weight gain accompanies molting ( Hiatt, 1948 ; Kurata, 1953 ).
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Change of wet body weights by methyl farnesoate (MF) treatment and unilateral eyestalk ablation (ESA). White and black circle represent initial weight and final weight, respectively. Two asterisks (**) are shown for the statistical difference (P < 0.01).
- Effect of treatments on ovarian maturation
To understand the effects of MF on maturation, GSI indices were calculated 31 days after treatment ( Fig. 3 ). All experimental groups had higher GSI values than the control group. The 1.0 μg MF group (0.33 ± 0.08) had GSI values threefold greater than the 0.1 μg MF group (0.10 ± 0.03), and was not significantly different from the ESA group (0.36 ± 0.14). Therefore, a high level of MF can induce ovarian maturation to the levels induced by ESA.
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Comparison of gonadosomatic indices (GSIs) in response to methyl farnesoate (MF) injection and unilateral eyestalk ablation (ESA). Statistical significance in each group was shown alphabetically (P < 0.05).
Histological analysis also indicated that both MF injection and ESA facilitated ovarian maturation ( Fig. 4 ). Unlike in the control group (immature stage), characteristics representative of the previtellogenic stage, with oocytes containing small yolk granules, were found in both the 1.0 μg MF and ESA groups ( Tinikul et al., 2011 ). In the 0.1- and 1.0-μg MF groups, early previtellogenic characteristics, in the form of small follicle cells, were also present and distributed around the periphery of the lobes ( Fig. 4 ). The effects of MF vary among species. No stimulatory effects have been found in Cherax quadricarinatus, Homarus americanus, Macrobrachium rosenbergii , and Triops longicaudatus . ( Table 2 ). Conversely, in Macrobrachium malcolmsonii ( Nagaraju et al., 2004 ), Oziotelphusa senex senex ( Reddy et al., 2004 ), and Penaeus indicus ( Nagaraju et al., 2002 ), MF administration resulted in gonad stimulation. In another study, feed containing MF induced maturation in Procambarus clarkii ( Laufer et al., 1998 ). These results suggest that reproductive endocrinology in decapod crustaceans is highly complex, and further research is required to establish a general and comprehensive understanding.
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Histology of ovaries 31 days after methyl farnesoate (MF) and eyestalk ablation treatment. Each ovary was stained with H&E, and observed in light microscope(ⅹ100). (A) Control female; (B) 0.1 μg MF treated female; (C) 1.0 μg MF treated female; (D) unilaterally eyestalk ablated female.
Effects of methyl farnesoate on crustacean reproduction
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+, gonad stimulation; –, gonad inhibition; NE, no effect.
The regulation of growth and ovarian development processes in crustaceans are related to the molting cycle. Molting regulation in crustaceans is known to be controlled primarily by ecdysteroids ( Wongsawang et al., 2005 ; Brown et al., 2009 ). The Y-organ is responsible for the synthesis and secretion of the inactive precursor compound, ecdysone, which is converted to 20E, the biologically active ecdysteroid ( Chang, 1985 ). This process is negatively regulated by the MIH, which is also secreted from the XO/SG complex ( Webster, 1998 ; Huberman, 2000 ). A positive correlation between ovary ecdysteroids levels and ovarian development has been demonstrated in the shore crab Carcinus maenas ( Lachaise et al., 1981 ). The XO/SG complex contains various types of CHH, including types I and II. These peptides are classified by gene structure and function. Type I peptides consist of CHH and CHH-related peptides, and type II peptides consist of MIH, gonad or vitellogenesis-inhibiting hormone (GIH or VIH, respectively), and the MOIH ( Chan et al., 2003 ; Fanjul-Moles, 2006 ).
Along with MIH, GIH/VIH is produced in the XO/SG complex (Van Herp and Soyez, 1997 ). In our study, ESA induced two physiological responses: the induction of 20E levels and the removal of GIH/VIH hormones. However, since both MIH and GIH/VIH are of the same CHH family type, their functions may be redundant. Hence, in some decapods, distinguishing MIH from GIH/VIH is problematic.
Eyestalk ablation may affect MF production. In an arthropod- specific second step, FA is converted to MF by P450 monooxygenase and farnesoic acid O-methyltransferase (FAMeT) ( Goldstein and Brown, 1990 ; Holford et al., 2004 ). Crustacean FAMeT catalyzes the methylation of FA to MF; cDNAs for this protein have been isolated from various crustacean species, including lobsters, shrimp, and crabs, and its expression is induced by ESA ( Gunawardene et al., 2002 ; Holford et al., 2004 ; Kuballa et al., 2007 ). Eyestalk ablation in spider crabs , Libinia emarginata , elevated the hemolymph MF concentration, increasing the GSI ( Jo et al., 1999 ). Furthermore, Laufer et al. (1987) reported that unilateral and bilateral ESA induced an increase of MF and stimulated ovarian growth in L. emarginata .
In conclusion, the high-dose MF treatment (1.0 μg) stimulated molting, growth, and ovarian maturation in L. vannamei, effects similar to those of ESA. The similar physiological effects of MF and ESA have raised questions in the field of crustacean reproductive endocrinology. Therefore, further research addressing the cooperative or synergic effects of MF and 20E on growth and reproduction is important for our understanding of crustacean reproductive endocrinology.
Acknowledgements
This work was supported by the Pukyong National University Research Abroad Fund in 2012 (CD 2011 0305).
References
Abdu U , Barki A , Karplus I , Barel S , Takac P , Yehezkel G , Laufer H , Sagi A 2001 Physiological effects of methyl farnesoate and pyriproxyfen on wintering female crayfish Cherax quadricarinatus Aquaculture http://dx.doi.org/10.1016/S0044-8486(01)00596-8 202 163 - 175
Bell TA , Lightner DV 1988 A Handbook of Normal Penaeid Shrimp Histology World Aquaculture Society Baton Rouge, LA, US
Bellés X , Martin D , Piulachs MD 2005 The mevalonate pathway and the synthesis of juvenile hormone in insects Annu Rev Entomol http://dx.doi.org/10.1146/annurev.ento.50.071803.130356 50 181 - 199
Borst DW , Laufer H , Landau M , Chang ES , Hertz WA , Baker FC , Schooley DA 1987 Methyl farnesoate and its role in crustacean reproduction and development Insect Biochem http://dx.doi.org/10.1016/0020-1790(87)90133-8 17 1123 - 1127
Borst DW , Ogan J , Tsukimura B , Claerhout T , Holford KC 2001 Regulation of the crustacean mandibular organ Am Zool http://dx.doi.org/10.1093/icb/41.3.430 41 430 - 441
Borst DW , Wainwright G , Rees HH 2002 In vivo regulation of the mandibular organ in the edible crab, Cancer pagurus Proc Biol Sci http://dx.doi.org/10.1098/rspb.2001.1870 269 483 - 490
Browdy C , Wyban J 1992 A Review of the Reproductive Biology of Penaeus Species: Perspectives on Controlled Shrimp Maturation Systems for High Quality Nauplii Production World Aquaculture Society Baton Rouge, LA, US Proceedings on the Special Session on Shrimp Farming 22 - 51
Brown MR , Sieglaff DH , Rees HH 2009 Gonadal ecdysteroidogenesis in Arthropoda: occurrence and regulation Annu Rev Entomol http://dx.doi.org/10.1146/annurev.ento.53.103106.093334 54 105 - 125
Chan SM , Gu PL , Chu KH , Tobe SS 2003 Crustacean neuropeptide genes of the CHH/MIH/GIH family: implications from molecular studies Gen Comp Endocrinol http://dx.doi.org/10.1016/S0016-6480(03)00263-6 134 214 - 219
Chang ES 1985 Hormonal control of molting in decapod Crustacea Am Zool http://dx.doi.org/10.1093/icb/25.1.179 25 179 - 185
Choy SC 1987 Growth and reproduction of eyestalk ablated Penaeus canaliculatus (Olivier, 1811) (crustacea: Penaeidae) J Exp Mar Biol Ecol http://dx.doi.org/10.1016/0022-0981(87)90111-0 112 93 - 107
Covi JA , Chang ES , Mykles DL 2009 Conserved role of cyclic nucleotides in the regulation of ecdysteroidogenesis by the crustacean molting gland Comp Biochem Physiol A Mol Integr Physiol http://dx.doi.org/10.1016/j.cbpa.2008.12.005 152 470 - 477
Emmerson WD 1980 Induced maturation of prawn Penaeus indicus Mar Ecol Prog Ser http://dx.doi.org/10.3354/meps002121 2 121 - 131
Fanjul-Moles ML 2006 Biochemical and functional aspects of crustacean hyperglycemic hormone in decapod crustaceans: review and update Comp Biochem Physiol C Toxicol Pharmacol http://dx.doi.org/10.1016/j.cbpc.2005.11.021 142 390 - 400
Goldstein JL , Brown MS 1990 Regulation of the mevalonate pathway Nature http://dx.doi.org/10.1038/343425a0 343 425 - 430
Gunawardene YI , Tobe SS , Bendena WG , Chow BK , Yagi KJ , Chan SM 2002 Function and cellular localization of farnesoic acid O-methyltransferase (FAMeT) in the shrimp, Metapenaeus ensis Eur J Biochem http://dx.doi.org/10.1046/j.1432-1033.2002.03048.x 269 3587 - 3595
Hiatt RW 1948 The biology of the lined shore crab, Pachygrapsus crassipes Randall Pac Sci 2 135 - 213
Holford KC , Edwards KA , Bendena WG , Tobe SS , Wang Z , Borst DW 2004 Purification and characterization of a mandibular organ protein from the American lobster, Homarus americanus: a putative farnesoic acid O-methyltransferase Insect Biochem Mol Biol http://dx.doi.org/10.1016/j.ibmb.2004.04.003 34 785 - 798
Homola E , Chang ES 1997 Distribution and regulation of esterases that hydrolyze methyl farnesoate in Homarus americanus and other crustaceans Gen Comp Endocrinol http://dx.doi.org/10.1006/gcen.1996.6850 106 62 - 72
Huberman A 2000 Shrimp endocrinology: a review Aquaculture http://dx.doi.org/10.1016/S0044-8486(00)00428-2 191 191 - 208
Hui JHL , Hayward A , Bendena WG , Takahashi T , Tobe SS 2010 Evolution and functional divergence of enzymes involved in sesquiterpenoid hormone biosynthesis in crustaceans and insects Peptides http://dx.doi.org/10.1016/j.peptides.2009.10.003 31 451 - 455
Jo QT , Laufer H , Biggers WJ , Kang HS 1999 Methyl farnesoate induced ovarian maturation in the spider crab, Libinia emarginata Invertebr Reprod Dev http://dx.doi.org/10.1080/07924259.1999.9652681 36 79 - 85
Juinio-Meñez MA , Ruinata J 1996 Survival, growth and food conversion efficiency of Panulirus ornatus following eyestalk ablation Aquaculture http://dx.doi.org/10.1016/S0044-8486(96)01371-3 146 225 - 235
Kuballa AV , Guyatt K , Dixon B , Thaggard H , Ashton AR , Paterson B , Merritt DJ , Elizur A 2007 Isolation and expression analysis of multiple isoforms of putative farnesoic acid O-methyltransferase in several crustacean species Gen Comp Endocrinol http://dx.doi.org/10.1016/j.ygcen.2006.07.020 150 48 - 58
Kurata H 1953 Studies on the age and growth of Crustacea Bull Hokkaido Reg Fish Res Lab 24 1 - 115
Lachaise F , Goudeau M , Hetru C , Kappler C , Hoffmann JA 1981 Ecdysteroids and ovarian development in the shore crab, Carcinus maenas Hoppe Seylers Z Physiol Chem http://dx.doi.org/10.1515/bchm2.1981.362.1.521 362 521 - 530
Laufer H , Borst D , Baker FC , Reuter CC , Tsai LW , Schooley DA , Carrasco C , Sinkus M 1987 Identification of a juvenile hormone-like compound in a crustacean Science http://dx.doi.org/10.1126/science.235.4785.202 235 202 - 205
Laufer H , Biggers WJ , Ahl JS 1998 Stimulation of ovarian maturation in the crayfish Procambarus clarkii by methyl farnesoate Gen Comp Endocrinol http://dx.doi.org/10.1006/gcen.1998.7109 111 113 - 118
Laufer H , Demir N , Pan X , Stuart JD , Ahl JSB 2005 Methyl farnesoate controls adult male morphogenesis in the crayfish, Procambarus clarkii J Insect Physiol http://dx.doi.org/10.1016/j.jinsphys.2005.02.007 51 379 - 384
Marsden G , Hewitt D , Boglio E , Mather P , Richardson N 2008 Methyl farnesoate inhibition of late stage ovarian development and fecundity reduction in the black tiger prawn, Penaeus monodon Aquaculture http://dx.doi.org/10.1016/j.aquaculture.2008.04.031 280 242 - 246
Mykles DL 2011 Ecdysteroid metabolism in crustaceans J Steroid Biochem Mol Biol http://dx.doi.org/10.1016/j.jsbmb.2010.09.001 127 196 - 203
Nagaraju G 2003 Mandibular organ: its role in the regulation of reproduction and molting in the crab, Oziotelphusa senex senex. Ph.D. Dissertation Sri Venkateswara University Tirupati, IN
Nagaraju GPC 2007 Is methyl farnesoate a crustacean hormone? Aquaculture http://dx.doi.org/10.1016/j.aquaculture.2007.05.014 272 39 - 54
Nagaraju GP 2011 Reproductive regulators in decapod crustaceans: an overview J Exp Biol http://dx.doi.org/10.1242/jeb.047183 214 3 - 16
Nagaraju GPC , Borst DW 2008 Methyl farnesoate couples environmental changes to testicular development in the crab Carcinus maenas J Exp Biol http://dx.doi.org/10.1242/jeb.019133 211 2773 - 2778
Nagaraju GPC , Ramamurthi R , Reddy PS , Harikumar VS . 2002 Recent Trends in Biotechnology Agrobios, IN Methyl farnesoate stimulates ovarian growth in Penaeus indicus 85 - 89
Nagaraju GPC , Suraj NJ , Reddy PS 2003 Methyl farnesoate stimulates gonad development in Macrobrachium malcolmsonii (H. Milne Edwards) (Decapoda, Palaemonidae) Crustaceana http://dx.doi.org/10.1163/156854003773123401 76 1171 - 1178
Nagaraju GPC , Prasad GLV , Reddy PS 2005 Isolation and characterization of mandibular organ inhibiting hormone from the eyestalks of freshwater crab, Oziotelphusa senex senex Int J Appl Sci Eng 3 61 - 68
Nakatsuji T , Lee CY , Watson RD 2009 Crustacean molt-inhibiting hormone: structure, function, and cellular mode of action Comp Biochem Physiology A Mol Integr Physiol http://dx.doi.org/10.1016/j.cbpa.2008.10.012 152 139 - 148
Paran BC , Fierro IJ , Tsukimura B 2010 Stimulation of ovarian growth by methyl farnesoate and eyestalk ablation in penaeoidean model shrimp, Sicyonia ingentis Burkenroad, 1938 Aquac Res http://dx.doi.org/10.1111/j.1365-2109.2010.02612.x 41 1887 - 1897
Ponnuchamy R , Reddy SR , Shakuntala K 1981 Effects of eyestalk ablation on growth and food conversion efficiency of the freshwater prawn Macrobrachium lanchesteri (de Man) Hydrobiologia http://dx.doi.org/10.1007/BF00006391 77 77 - 80
Reddy PR , Nagaraju GPC , Reddy PS 2004 Involvement of methyl farnesoate in the regulation of molting and reproduction in the freshwater crab Oziotelphusa senex senex J Crust Biol http://dx.doi.org/10.1651/C-2478 24 511 - 515
Riley LG , Tsukimura B 1998 Yolk protein synthesis in the riceland tadpole shrimp, Triops longicaudatus, measured by in vitro incorporation of3H-leucine J Exp Zool http://dx.doi.org/10.1002/(SICI)1097-010X(19980615)281:3<238::AID-JEZ10>3.0.CO;2-7 281 238 - 247
Rodríguez EM , López Greco LS , Medesani DA , Laufer H , Fingerman M 2002 Effect of methyl farnesoate, alone and in combination with other hormones, on ovarian growth of the red swamp crayfish, Procambarus clarkii, during vitellogenesis Gen Comp Endocrinol http://dx.doi.org/10.1006/gcen.2001.7724 125 34 - 40
Salma U , Uddowla MH , Kim M , Kim JM , Kim BK , Baek HJ , Park H , Mykles DL , Kim HW 2012 Five hepatopancreatic and one epidermal chitinases from a pandalid shrimp (Pandalopsis japonica): cloning and effects of eyestalk ablation on gene expression Comp Biochem Physiol B Biochem Mol Biol http://dx.doi.org/10.1016/j.cbpb.2011.11.005 161 197 - 207
Santiago AC 1977 Successful spawning of cultured Penaeus monodon Fabricius after eyestalk ablation Aquaculture http://dx.doi.org/10.1016/0044-8486(77)90111-9 11 185 - 196
Tinikul Y , Poljaroen J , Nuurai P , Anuracpreeda P , Chotwiwatthanakun C , Phoungpetchara I , Kornthong N , Poomtong T , Hanna PJ , Sobhon P 2011 Existence and distribution of gonadotropinreleasing hormone-like peptides in the central nervous system and ovary of the Pacific white shrimp, Litopenaeus vannamei Cell Tissue Res http://dx.doi.org/10.1007/s00441-010-1112-3 343 579 - 593
Tsubota T , Minakuchi C , Nakakura T , Shinoda T , Shiotsuki T 2010 Molecular characterization of a gene encoding juvenile hormone esterase in the red flour beetle, Tribolium castaneum Insect Mol Biol http://dx.doi.org/10.1111/j.1365-2583.2010.01019.x 19 527 - 535
Tsukimura B , Kamemoto FI , Borst DW 1993 Cyclic nucleotide regulation of methyl farnesoate synthesis by the mandibular organ of the lobster, Homarus americanus J Exp Zool http://dx.doi.org/10.1002/jez.1402650412 265 427 - 431
Tsukimura B , Nelson WK , Linder CJ 2006 Inhibition of ovarian development by methyl farnesoate in the tadpole shrimp, Triops longicaudatus Comp Biochem Physiol A Mol Integr Physiol http://dx.doi.org/10.1016/j.cbpa.2006.02.015 144 135 - 144
Van Herp F , Soyez D , Adiyodi KG , Adiyodi RG. 1997 Progress in Reproductive Endocrinology, Part A Oxford and IBH Publishing Co. New Dehli, IN Arthropoda-crustacea. Reproductive biology in invertebrates: Arthropoda-Crustacea 247 - 275
Wainwright G , Webster SG , Wilkinson MC , Chung JS , Rees HH 1996 Structure and significance of mandibular organ-inhibiting hormone in the crab, Cancer pagurus. Involvement in multihormonal regulation of growth and reproduction J Biol Chem http://dx.doi.org/10.1074/jbc.271.22.12749 271 12749 - 12754
Webster SG , Coast GM , Webster SG. 1998 Recent Advances in Anthropod Endocrinology Cambridge University Press Cambridge, GB Neuropeptides inhibiting growth and reproduction in crustaceans 33 - 52
Wilder NM , Okumura T , Suzuki Y , Fusetani N , Aida K 1994 Vitellogenin production induced by eyestalk ablation in juvenile giant freshwater prawn Macrobrachium rosenbergii and trial methyl farnesoate administration Zool Sci 11 45 - 53
Wongsawang P , Phongdara A , Chanumpai A , Chotigeat W 2005 Detection of CHH/GIH activity in fractionated extracts from the eyestalk of Banana prawn Songklanakarin J Sci Tech 27 789 - 798
Yano I 1984 Induction of rapid spawning in kuruma prawn, Penaeus japonicus, through unilateral eyestalk enucleation Aquaculture http://dx.doi.org/10.1016/0044-8486(84)90195-9 40 265 - 268